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Polar Biology

, Volume 30, Issue 2, pp 219–225 | Cite as

Geographic variation in the immunoglobulin levels in pygoscelid penguins

  • Andrés BarbosaEmail author
  • Santiago Merino
  • Jesús Benzal
  • Javier Martinez
  • Sonia García-Fraile
Original Paper

Abstract

Antarctic organisms, including penguins, are susceptible to parasites and pathogens. Effects of infestation could differ in different locations along a geographical gradient from north to south consistent with conditions that affect the prevalence and virulence of parasites and pathogens. The immune system, including immunoglobulins as the main component of the humoral immune response, is the major way by which organisms confront infestation. We investigated the variation in immunoglobulin levels in three species of antarctic penguins (Pygoscelis antarctica, Pygoscelis papua, and Pygoscelis adeliae) along a geographical gradient from King George Island (62°15′S) to Avian Island (67°46′S). We found that immunoglobulin levels increased northwards in all the three species. This could indicate a higher impact of parasites and/or pathogens relative to the existing gradient in temperatures along this coast. Changing temperatures, consistent with global climate change, could be altering the ecology of parasite or pathogen infestation within the biota of northern Antarctica. We have also found marginal differences in immunoglobulin levels between sexes in both chinstrap and gentoo penguins.

Keywords

Antarctic Peninsula Immunoglobulin Level Northern Population Gentoo Penguin Pied Flycatcher 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This study has been funded by the Acción Especial project REN2001-5004/ANT of the Spanish Ministry of Education and Science. The project CGL2004-01348/ANT supported AB while the paper was written. We very much appreciated the hospitality and logistic support of the Spanish Antarctic Bases “Juan Carlos I,” “Gabriel de Castilla” and the Spanish Polar Ship “Hesperides” and specially the Spanish Polar Ship “Las Palmas” which provided us the logistic support and transport to the localities. We thank Elena Arriero and Rafa Barrientos for laboratory assistance with molecular sexing. We also thank two anonymous referees for their comments that improved early versions of the manuscript.

References

  1. Barbosa A, Moreno E (2002) Sex differences in t-cell-mediated immune response in wintering great tits Parus major. Avian Sci 2:99–102Google Scholar
  2. Barbosa A, Moreno E (2004) Cell-mediated immune response affects food intake but no body mass: an experiment with wintering great tits. Ecoscience 11:305–309Google Scholar
  3. Bennett GF, Squires-Parsons D, Siikamäki P, Huhta E, Allander K, Hillström L (1995) A comparison of the blood parasites of three Fenno-Scandian populations of the pied flycatcher Ficedula hypoleuca. J Avian Biol 26:33–38Google Scholar
  4. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127CrossRefPubMedGoogle Scholar
  5. Boutette JB, Ramsay EC, Potgieter LND, Kania SA (2002) An improved polymerase chain reaction-restriction fragment length polymorphism assay for gender identification in birds. J Avian Med Surg 16:198–202CrossRefGoogle Scholar
  6. Chapell MA, Souza SL (1988) Thermoregulation, gas exchange, and ventilation in Adelie penguins (Pygoscelis adeliae). J Comp Physiol B 157:783–790CrossRefGoogle Scholar
  7. Clayton DH, Moore J (1997) Host–parasite evolution: general principles and avian models. Oxford University Press, OxfordGoogle Scholar
  8. Dupas S, Boscaro R (1999) Geographic variation and evolution of immunosuppressive genes in a Drosophila parasitoid. Ecography 22:284–291CrossRefGoogle Scholar
  9. Ellegren H (1996) First gene on the avian W chromosome (CHD) provides a tag for universal sexing of non-ratite birds. Proc R Soc Lond B 263:1635–1641Google Scholar
  10. Fellowes MDE, Godfray HCJ (2000) The evolutionary ecology of resistance to parasitoids by Drosophila. Heredity 84:1–8CrossRefPubMedGoogle Scholar
  11. Gardner H, Kerry K, Riddle M, Brouwer S, Gleeson L (1997) Poultry virus infection in Antarctic penguins. Nature 387:245CrossRefPubMedGoogle Scholar
  12. Gauthier-Clerc M, Eterradossi N, Toquin D, Guittet M, Kuntz G, Le Maho Y (2002) Serological survey of the king penguin, Aptenodytes patagonicus, in Crozet archipelago for antibodies to infectious bursal disease influenza A and Newcastle disease viruses. Polar Biol 25:316–319Google Scholar
  13. Grasman KA (2002) Assessing immunological function in toxicological studies of avian wildlife. Integr Comp Biol 42:34–42CrossRefGoogle Scholar
  14. Grossman CJ (1984) Regulation of immune system by sex steroids. Endocr Rev 5:435–455PubMedGoogle Scholar
  15. Gustaffson L, Nordling D, Andersson MS, Sheldon BC, Qvarstrom A (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Phil Trans R Soc Lond B 346:323–331Google Scholar
  16. Johnsen TS, Zuk M (1999) Parasites and tradeoffs in the immune response of female red jungle fowl. Oikos 86:487–492Google Scholar
  17. Jones HI, Shellam GR (1999) The occurrence of blood-inhabiting protozoa in captive and free-living penguins. Polar Biol 21:5–10CrossRefGoogle Scholar
  18. Kerry K, Riddle M, Clarke K (1999) Diseases of Antarctic wildlife. A report for SCAR and COMNAP. SCARGoogle Scholar
  19. King JC, Turner J, Marshall GJ, Connolley WM, Lachlan-Cope TA (2003) Antarctic Peninsula climate variability and its causes as revealed by analysis of instrumental records. AGU Antarct Res Ser 79:17–30Google Scholar
  20. Kraaijeveld AR, Godfray HCJ (1999) Geographic patterns in the evolution of resistance and virulence in Drosophila and its parasitoids. Am Nat 153:S61–S74CrossRefGoogle Scholar
  21. Lindgren E (1998) Climate change, tick-borne encephalitis and vaccination needs in Sweden—a prediction model. Ecol Modell 110:55–63CrossRefGoogle Scholar
  22. Lindgren E, Talleklint L, Polfeldt T (2000) Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ Health Perspect 108:119–123PubMedGoogle Scholar
  23. Martínez J, Tomás G, Merino S, Arriero E, Moreno J (2003) Detection of serum immunoglobulins in wild birds by direct ELISA: a methodological study to validate the technique in different species using antichicken antibodies. Funct Ecol 17:700–706CrossRefGoogle Scholar
  24. McGraw KJ, Ardia DR (2005) Sex differences in carotenoid status and immune performance in zebra finches. Evol Ecol Res 7:251–262Google Scholar
  25. Meloni S, Mazzini M, Buonocore F, Scapigliati G (2000) Humoral immunity in Antarctic fish: serum immunoglobulin analysis in seven species and antigen-induced response in Trematomus bernacchii (Teleostea, Notothenioidea). Ital J Zool 67:79–83CrossRefGoogle Scholar
  26. Merila J, Björklund M, Bennett GF (1995) Geographic and individual variation in haematozoan infections in the greenfinch, Carduelis chloris. Can J Zool 73:1798–1804CrossRefGoogle Scholar
  27. Merino S, Barbosa A, Moreno J, Potti J (1997) Absence of haematozoa in a wild chinstrap penguin Pygoscelis antarctica population. Polar Biol 18:227–228CrossRefGoogle Scholar
  28. Merino S, Martínez J, Møller AP, Sanabria L, de Lope F, Pérez J, Rodríguez-Caabeiro F (1999) Phytohaemagglutinin injection assay and physiological stress in nestling house martins. Anim Behav 58:219–222CrossRefPubMedGoogle Scholar
  29. Møller AP (1998) Evidence of larger impact of parasites on host in the tropics: investment in immune function within and outside tropics. Oikos 82:265–270CrossRefGoogle Scholar
  30. Møller AP (2002) North Atlantic Oscillation (NAO) effects of climate on the relative importance of first and second clutches in a migratory passerine birds. J Anim Ecol 71:201–210CrossRefGoogle Scholar
  31. Møller AP, Erritzoe J (1998) Host immune defence and migration in birds. Evol Ecol 12:945–953CrossRefGoogle Scholar
  32. Møller AP, Erritzoe J (2001) Dispersal, vaccination and regression of immune defence organs. Ecol Lett 4:484–490CrossRefGoogle Scholar
  33. Møller AP, Erritzoe J (2002) Coevolution of host immune defence and parasite-induced mortality: relative spleen size and mortality in altricial birds. Oikos 99:95–100CrossRefGoogle Scholar
  34. Møller AP, Erritzoe J (2003) Climate, body condition and spleen size in birds. Oecologia 442:621–626CrossRefGoogle Scholar
  35. Møller AP, Sorci G, Erritzoe J (1998) Sexual dimorphism in immune defense. Am Nat 152:605–619CrossRefPubMedGoogle Scholar
  36. Møller AP, Merino S, Brown CR, Robertson RJ (2001) Immune defense and host sociality: a comparative study or swallows and martins. Am Nat 158:136–145CrossRefPubMedGoogle Scholar
  37. Morales J, Moreno J, Merino S, Tomás G, Martínez J, Garamszegi LZ (2004) Associations between immune parameters, parasitism, and stress in breeding pied flycatcher (Ficedula hypoleuca) females. Can J Zool 82:1484–1492CrossRefGoogle Scholar
  38. Moreno J, de León A, Fargallo JA, Moreno E (1998) Breeding time, health and immune response in the chinstrap penguin Pygoscelis antarctica. Oecologia 115:312–319CrossRefGoogle Scholar
  39. Moreno J, Potti J, Yorio P, Garcia Borboroglu P (2001) Sex differences in cell-mediated immunity in the magellanic penguin Spheniscus magellanicus. Ann Zool Fenn 38:111–116Google Scholar
  40. Nunn CL (2002) Spleen size, disease risk and sexual selection: a comparative study in primates. Evol Ecol Res 4:91–107Google Scholar
  41. Nunn CL, Gittleman JL, Antonovics J (2000) Promiscuity and the primate immune system. Science Wash 290:1168–1170CrossRefGoogle Scholar
  42. Olson JJ (2002) Antarctica: a review of recent medical research. Trends Pharmacol Sci 23:487–490CrossRefPubMedGoogle Scholar
  43. Ots I, Horak P (1998) Health impact of blood parasites in breeding great tits. Oecologia 116:441–448CrossRefGoogle Scholar
  44. Ots I, Kerimov AB, Ivankina EV, Ilyina TA, Horak P (2001) Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc Lond B 268:1175–1181CrossRefGoogle Scholar
  45. Pastoret P, Gabriel P, Bazin H, Govaerts A (1998) Handbook of vertebrate immunology. Academic, San DiegoGoogle Scholar
  46. Potti J, Moreno J, Yorio P, Briones V, Garcia-Borboroglu P, Villar S, Ballesteros C (2002) Bacteria divert resources from growth for magellanic penguin chicks. Ecol Lett 5:709–714CrossRefGoogle Scholar
  47. Raberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc R Soc Lond B 265:1637–1641CrossRefGoogle Scholar
  48. Raberg L, Nilsson JA, Ilmonen P, Stjernman M, Hasselquist D (2000) The cost of an immune response: vaccination reduces parental effort. Ecol Lett 3:382–386CrossRefGoogle Scholar
  49. Redig PT, Lawler EM, Schwartz S, Dunnette JL, Stephenson B, Duke GE (1991) Effects of chronic exposure to sublethal concentrations of lead acetate on heme synthesis and immune function in red-tailed hawks. Arch Environ Contam Toxicol 21:72–77CrossRefPubMedGoogle Scholar
  50. Roitt I, Brostoff J, Male D (1996) Immunology. Mosby, LondonGoogle Scholar
  51. Saino N, Martinelli R, Møller AP (2001) Immunoglobulin plasma concentration in relation to egg laying and mate ornamentation of female barn swallows (Hirundo rustica). J Evol Biol 14:95–109CrossRefGoogle Scholar
  52. Sladen WJL (1954) Penguin in the wild and in captivity. Avic Mag 60:132–142Google Scholar
  53. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohemagglutinin skin testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572CrossRefGoogle Scholar
  54. Snoeijs T, Dauwe T, Pinxten R, Vandesande F, Eens M (2004) Heavy metal exposure affects the humoral immune response in a free-living small songbird, the Great Tit (Parus major). Arch Environ Contam Toxicol 46:399–404CrossRefPubMedGoogle Scholar
  55. Sol D, Jovani R, Torres J (2000) Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23:307–314CrossRefGoogle Scholar
  56. Sutherst RW (2001) The vulnerability of animal and human health to parasites under global change. Int J Parasitol 31:933–948CrossRefPubMedGoogle Scholar
  57. Szep T, Møller AP (1999) Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent–offspring conflict? Oecologia 119:9–15CrossRefGoogle Scholar
  58. Taylor JRE (1985) Ontogeny of thermoregulation and energy metabolism in pygoscelid penguin chicks. J Comp Physiol 155B:615–627Google Scholar
  59. Tella JL, Scheuerlein A, Ricklefs RE (2002) Is cell mediated immunity related to the evolution of life-history strategies in birds? Proc R Soc Lond B 269:1059–1066CrossRefGoogle Scholar
  60. Terres G, Morrison SL, Habricht GS (1968) A quantitative difference in the immune response between male and female mice. Proc Soc Exp Biol Med 47:273Google Scholar
  61. Turner J, Colwell SR, Marshall GJ, Lachlan-Cope TA, Carleton AM, Jones PD, Lagun V, Reid PA, Iagovkina S (2004) The SCAR READER project: toward a high-quality database of mean Antarctic meteorological observations. J Clim 17:2890–2898CrossRefGoogle Scholar
  62. Wakelin D, Apanius V (1997) Immune defence: genetic control. In: Clayton DH, Moore J (eds) Host–parasite evolution. General principles and avian models. Oxford University Press, Oxford, pp 30–58Google Scholar
  63. Wikel SK (1996) The immunology of host-ectoparasitic arthropod relationships. CAB International, Wallingford, UKGoogle Scholar
  64. Williams TD (1995) The penguins. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Andrés Barbosa
    • 1
    Email author
  • Santiago Merino
    • 2
  • Jesús Benzal
    • 1
  • Javier Martinez
    • 3
  • Sonia García-Fraile
    • 2
  1. 1.Departamento de Ecología Funcional y EvolutivaEstación Experimental de Zonas Áridas, CSIC, C/General Segura, 1AlmeriaSpain
  2. 2.Departamento de Ecología EvolutivaMuseo Nacional de Ciencias Naturales, CSIC, C/José Gutiérrez Abascal, 2MadridSpain
  3. 3.Departamento de Microbiología y Parasitología, Facultad de FarmaciaUniversidad de Alcalá de HenaresAlcala de HenaresSpain

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